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Thesis Body-No Codes-Final The plasticity of life histories during larval development and metamorphosis, using amphibians as study organisms. Patrick Thomas Walsh Presented for the degree of Doctor of Philosophy Division of Environmental and Evolutionary Biology Institute of Biomedical and Life Sciences University of Glasgow December 2007 ©Patrick Thomas Walsh 2007 Candidate’s declaration I declare that the work presented in this study is entirely my own unless otherwise stated and that it is of my own composition. No part of this thesis has been submitted for any other degree. Patrick Thomas Walsh December 2007 Acknowledgements Acknowledgements First, and foremost, I would like to thank, equally but for very different reasons, both of my supervisors, Professors Roger Downie and Pat Monaghan. I would like to thank Roger for his ‘open-door’ policy that has allowed many frank and helpful discussions about the contents of this thesis. Additionally, for allowing me the opportunity to greatly expand my CV by being given the option to help with the supervision of honours’ students and as much demonstrating as I could find time for. I would like to thank Pat for a great deal of patience and attention to detail, providing a perfect contrast to my frantic writing style and usually questionable grammatical knowledge. The excellent feedback received by her throughout my PhD has taught me to think more critically and write more concisely. I also need to thank Pat for the open invitation to her house to sample her pond for tadpoles throughout the year, and for often delivering the tadpoles directly to the department. I am hugely indebted to the Carnegie Trust for the Universities of Scotland for providing me with the funding for this studentship and the two small project grants, Universities UK for covering the extortionate over-seas fees, and the Glasgow Natural History Society for grants to purchase equipment. I would also like to thank a number of staff members in the Division, without whom this thesis most certainly would not have been possible. Firstly, I would like to thank Graeme Adams for allowing me to have some time available to travel home to the US and not have to come back to thousands of dead tadpoles. Thanks go to John Laurie and June Freel, whose understanding of archaic pieces of equipment in the Graham Kerr basement allowed much of the work report to be carried out. I particularly would like to thank John Laurie for his patience in helping me to find enough space to meet my ever- Acknowledgements changing needs for constant temperature rooms. I thank Pat McLaughlin for allowing me to pinch various pieces of laboratory equipment. Thanks also go to Dan Haydon, who went above and beyond the call of duty as my assessor, for his feedback on early drafts of chapters. I also extend thanks to Jane Harrison, the Botanic Gardens and the members of the Kirklee Allotments for allowing me to use their ponds to sample for tadpoles. Thanks go to Isobel Maynard, Archie McClymont, Bernie Zonfrillo and Deborah McNeill for helping in acquiring all the tadpoles used in this study. There are also a number of people, around the department, that I would like to thank for making my time, not spent in the laboratory and field, enjoyable. This includes the many office-mates that have come and gone, particularly the many helpful chats with Claire Stamper and Liliana D’Alba, but extends to all the people that found the time to go for a drink on a Friday. Finally, but also most importantly, I would like to thank my wife Rachel for her constant support and encouragement and occasional assistance in the field, laboratory and reading over drafts. I also thank my parents for their encouragement throughout my PhD and in all my education leading towards this point. Contents Contents Abstract 1 Chapter 1: General Introduction 4 Chapter 2: Plasticity of the duration of metamorphosis in the African clawed toad 18 Abstract 18 Introduction 19 Methods and Materials 21 Results 26 Discussion 28 Chapter 3: Predation-induced plasticity in metamorphic duration in Xenopus laevis 38 Abstract 38 Introduction 39 Methods and Materials 41 Results 45 Discussion 47 Chapter 4: Temperature mediated morphology changes during metamorphic climax in the African clawed frog, Xenopus laevis 55 Abstract 55 Introduction 56 Methods and Materials 58 Results 59 Discussion 61 Chapter 5: The effects of temperature and food availability on the over-wintering of Rana temporaria tadpoles 68 Contents Abstract 68 Introduction 69 Methods and Materials 71 Results 73 Discussion 75 Chapter 6: The timing and pattern of larval development in over-wintering Rana temporaria tadpoles at a field site 84 Abstract 84 Introduction 85 Methods and Materials 87 Results 90 Discussion 93 Chapter 7: The effect of water depth on development and metamorphosis in two anuran larvae: Rana temporaria and Bufo bufo 105 Abstract 105 Introduction 107 Methods and Materials 110 Results 113 Discussion 115 Chapter 8: General discussion 123 References 141 Appendix 1: National survey of larval over-wintering 189 Appendix 2: Latitudinal variation in the proportion of over-wintering larvae 192 Appendix 3: Other outputs 194 List of tables List of tables Table 2.1: Starting measurements of different temperature treatment groups (ANOVA results displayed; NS indicates non-significant difference) 33 Table 3.1: Results of GLM analysis for the juvenile mass and structural size measurements of individuals that completed metamorphosis in the presence or absence of a predator and among the three temperature treatments. The interaction term was not significant (p > 0.27) and is not included. The holding tank that individuals originated from was not found to be significant in any of the analyses. 50 Table 3.2: Results of GLM analysis of locomotor performance of individuals at mid-metamorphosis and at the completion of metamorphosis in relation to predator and temperature treatments. The interaction between temperature and predator treatment were non-significant (p > 0.37) and removed. 50 Table 4.1: Initial measurements of mass, SVL and head width, and the duration of metamorphosis across the three temperature treatments. Data are presented as means (SE). Masses and lengths are provided in mg and mm, respectively. Durations of metamorphosis are presented as days since metamorphosis commenced. Degrees of freedom for GLM results are F 2,185 for temperature and interaction term and F 1,185 for year. 65 Table 5.1: Tadpole survivial during the experiment for each treatment group. The number of surviving tadpoles is given as the number of individuals successfully completing metamorphosis prior to the onset of winter plus the number of pre-metamorphic tadpoles at the onset of winter. Mean List of tables survival rate (± SE) as a percentage of the initial number is also given for each treatment group. The total number of individuals over-wintering and the mean percentage of surviving tadpoles over-wintering in each treatment group are also given. 81 Table 5.2: Regression analysis of development in Rana temporaria tadpoles from the start of the experiment until week 11 (* < 0.0001), where B is the slope of the regression equation (± SE). Differences in df are due to mortality during the course of the experiment. 81 Table 6.1: Monthly mean mass and snout-vent lengths of individuals from Drumtian pond. Analysis of normality of monthly mass, SVL and developmental stage is displayed as the Shaprio-Wilk statistic, with p values (* < 0.05, ** < 0.01, *** < 0.001, NS = non-significant result). Significant p-values denoting deviation from normality are given in bold. 98 Table 6.2: Monthly mean (± SE) mass (mg) and snout-vent length (mm) of individuals from the high and low food treatments in the laboratory. Analysis of normality is displayed as the Shaprio-Wilk statistic: NS = non-significant result, * < 0.05. 98 Table 7.1: Starting mass, SVL and developmental stage of different depth treatments for both R. temporaria and B. bufo , including results for t-tests for comparison between the depth treatments (df = 98). 120 Table 7.2: Mean mass (mg), SVL (mm) and Gosner stage of Rana temporaria (day 31) and Bufo bufo (day 36) for the shallow and deep treatments, including results for t-tests for comparison between depth treatments. List of tables Differences in the df between analyses is due the use of unequal variance t-tests (NS: not significant, * < 0.05, ** < 0.001). 120 Table 7.3: Mean frequency of trips to the surface (trips h -1) in Rana temporaria and Bufo bufo , for each stage grouping, in 0.2 m and 1 m deep tanks. Values are given as mean ± SE. Analyses from Mann-Whitney test of differences between the depth treatments at each stage group are given (Z) (NS: not significant, * < 0.05, ** < 0.005). P value thresholds are based on the Bonferroni corrected α–values. Analyses from Kruskal-Wallis H tests comparing the different stage groups within a depth treatment are presented as the X 2 value. 121 Table 8.1: The developmental stage used by studies on plasticity in anuran larval duration to signify the conclusion of larval development and whether the study provided any data on metamorphic duration. Studies that performed trials with post-metamorphic individuals are marked with an asterisk. 138 List of figures List of figures. Figure 2.1: Duration of metamorphosis in days (± SE) for the three temperature treatments. 34 Figure 2.2: Duration of metamorphosis in days in relation to body condition at the onset of metamorphosis (18ºC: ●, solid line; 24ºC: ○, dashed line, 30ºC: ▼, dotted line) 35 Figure 2.3: Decrease in mean tail length (± SE) through metamorphosis = 31 .437 2 (18°C: y − , r = 76.8%, p < 0.001; 24°C: 1 + e(( x .4 188 .0/) 653 ) = 31 .692 2 = 32 .627 y − , r = 85.7%, p < 0.001; 30°C: y − , 1 + e(( x .2 533 .0/) 289 )) 1 + e(( x .2 335 .0/) 319 ) r2 = 80.1%, p < 0.001) 36 Figure 2.4: Burst swimming speed (± SE) at different developmental stages.
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